Department of Biological Science, Florida State University, Tallahassee, FL, 32306, USA.
Department of Psychology, Florida State University, Tallahassee, FL, 32306, USA.
Sci Rep. 2023 Jul 7;13(1):11020. doi: 10.1038/s41598-023-37521-2.
In socially monogamous prairie voles (Microtus ochrogaster), parental behaviors not only occur in mothers and fathers, but also exist in some virgin males. In contrast, the other virgin males display aggressive behaviors towards conspecific pups. However, little is known about the molecular underpinnings of this behavioral dichotomy, such as gene expression changes and their regulatory mechanisms. To address this, we profiled the transcriptome and DNA methylome of hippocampal dentate gyrus of four prairie vole groups, namely attacker virgin males, parental virgin males, fathers, and mothers. While we found a concordant gene expression pattern between parental virgin males and fathers, the attacker virgin males have a more deviated transcriptome. Moreover, numerous DNA methylation changes were found in pair-wise comparisons among the four groups. We found some DNA methylation changes overlapping with transcription differences, across gene-bodies and promoter regions. Furthermore, the gene expression changes and methylome alterations are selectively enriched in certain biological pathways, such as Wnt signaling, which suggest a canonical transcription regulatory role of DNA methylation in paternal behavior. Therefore, our study presents an integrated view of prairie vole dentate gyrus transcriptome and epigenome that provides a DNA epigenetic based molecular insight of paternal behavior.
在社会性一夫一妻制的草原田鼠（Microtus ochrogaster）中，亲代行为不仅发生在母亲和父亲身上，也存在于一些处女雄性中。相比之下，其他的处女雄性则对同种幼崽表现出攻击性行为。然而，对于这种行为二分法的分子基础，如基因表达变化及其调控机制，我们知之甚少。为了解决这个问题，我们对四个草原田鼠群体的海马齿状回的转录组和 DNA 甲基化组进行了分析，这四个群体分别是：攻击型处女雄性、有亲代行为的处女雄性、父亲和母亲。虽然我们发现有亲代行为的处女雄性和父亲之间存在一致的基因表达模式，但攻击型处女雄性的转录组则有更大的偏差。此外，在这四个群体之间的两两比较中，我们发现了许多 DNA 甲基化变化。我们发现了一些 DNA 甲基化变化与基因体和启动子区域的转录差异重叠。此外，基因表达变化和甲基组改变在特定的生物学途径中被选择性富集，如 Wnt 信号通路，这表明 DNA 甲基化在父性行为中具有典型的转录调控作用。因此，我们的研究提供了一个草原田鼠齿状回转录组和表观基因组的综合视图，为父性行为提供了基于 DNA 表观遗传学的分子见解。
